Kv7 channels regulate pairwise spiking covariability in health and disease

Journal of Neurophysiology

Volumn 112, Issue 2, 2014, Pages 340-352

  Ocker, Gabriel Koch ^a,c   Doiron, Brent ^b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CENTER FOR THE NEURAL BASIS OF COGNITION   (United States)

Author keywords

Model; Model neurons; Noise correlations; Potassium channels; Synchrony

Indexed keywords

POTASSIUM CHANNEL KV7; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNQ;

ACTION POTENTIAL; ARTICLE; CONCEPTUAL FRAMEWORK; COVARIANCE; FOURIER TRANSFORMATION; HEALTH; HYPERACTIVITY; MEMBRANE POTENTIAL; NEGATIVE FEEDBACK; NERVE CELL; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NEUROMODULATION; POTASSIUM CONDUCTANCE; POWER SPECTRUM; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SINGLE UNIT ACTIVITY; SPIKE WAVE; STEADY STATE; ANIMAL; BIOLOGICAL MODEL; EPILEPSY; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; EPILEPSY; HUMANS; KCNQ POTASSIUM CHANNELS; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS;

EID: 84904302750     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00084.2014     Document Type: Article

References (79)

1. Abbott LF, van Vreeswijk C. Asynchronous states in networks of pulsecoupled oscillators. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 48: 1483-1490, 1993.
2. Abbott LF, Dayan P. The effect of correlated variability on the accuracy of a population code. Neural Comput 11: 91-101, 1999.
3. Abouzeid A, Ermentrout B. Correlation transfer in stochastically driven neural oscillators over long and short time scales. Phys Rev E Stat Nonlin Soft Matter Phys 84: 061914, 2011.
4. Adibi M, McDonald JS, Clifford CW, Arabzadeh E. Adaptation improves neural coding efficiency despite increasing correlations in variability. J Neurosci 33: 2108-2120, 2013.
5. Aiken S, Lampe B, Murphy P, Brown B. Reduction of spike frequency adaptation and block of m-current in rat CA1 pyramidal neurones by linopirdine (DuP 996), a neurotransmitter release enhancer. Br J Pharmacol 115: 1163-1168, 1995.
6. Averbeck BB, Latham PE, Pouget A. Neural correlations, population coding and computation. Nat Rev Neurosci 7: 358-366, 2006.
7. Barreiro A, Thilo E, Shea-Brown E. A-current and type 1/type 2 transition determine collective spiking from common input. J Neurophysiol 108: 1631-1645, 2012.
8. Benda J, Herz AV. A universal model for spike-frequency adaptation. Neural Comput 15: 2523-2564, 2003.
9. Benda J, Maler L, Longtin A. Linear vs. nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds. J Neurophysiol 104: 2806-2820, 2010.
10. Brickley S, Revilla V, Cull-Candy S, Wisden W, Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409: 88-92, 2001.
11. Brown DA, Passmore GM. Neural KCNQ (kv7) channels. Br J Pharmacol 156: 1185-1195, 2009.
12. Burkitt AN, Meffin H, Grayden DB. Study of neuronal gain in a conductance-based leaky integrate-and-fire neuron model with balanced excitatory and inhibitory synaptic input. Biol Cybern 89: 119-125, 2003.
13. Cohen MR, Kohn A. Measuring and interpreting neuronal correlations. Nat Neurosci 14: 811-819, 2011.
14. Cooper E, Jan L. M-channels neurological disease, neuromodulation and drug development. Arch Neurol 60: 496-500, 2003.
15. + channel mutation in benign neonatal convulsions and centrotemporal spikes. Neurology 61: 131-134, 2003.
16. Cox D, Isham V. Point Processes Monographs on Statistics and Applied Probability. New York: CRC, 1980.
17. Cudmore RH, Fronzaroli-Molinieres L, Giraud P, Debanne D. Spike-time precision and network synchrony are controlled by the homeostatic regulation of the D-type potassium current. J Neurosci 30: 12885-12895, 2010.
18. de la Rocha J, Doiron B, Shea-Brown E, Josic K, Reyes A. Correlation between neural spike trains increases with firing rate. Nature 448: 802-806, 2007.
19. Delmas P, Brown DA. Pathways modulating neural KCNQ/M (kv7) potassium channels. Nat Rev Neurosci 6: 850-862, 2005.
20. Desai NS, Rutherford LC, Turrigiano GG. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2: 515-520, 1999.
21. Doiron B, Longtin A, Berman N, Maler L. Subtractive and divisive inhibition: effect of voltage-dependent inhibitory conductances and noise. Neural Comput 13: 227-248, 2001.
22. Ermentrout GB. Linearization of f-i curves by adaptation. Neural Comput 10: 1721-1729, 1998.
23. Fan Y, Fricker D, Brager D, Chen X, Lu H, Chitwood R, Johnston D. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in IH. Nat Neurosci 8: 1542-1551, 2005.
24. Farkhooi F, Muller E, Nawrot MP. Adaptation reduces variability of the neuronal population code. Phys Rev E Stat Nonlin Soft Matter Phys 83: 050905, 2011.
25. Fisch K, Schwalger T, Lindner B, Herz AV, Benda J. Channel noise from both slow adaptation currents and fast currents is required to explain spike-response variability in a sensory neuron. J Neurosci 32: 17332-17344, 2012.
26. Fourcaud N, Brunel N. Dynamics of the firing probability of noisy integrateand-fire neurons. Neural Comput 14: 2057-2110, 2002.
27. Fourcaud-Trocme N, Hansel D, van Vreeswijk C, Brunel N. How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23: 11628-11640, 2003.
28. Galan R, Fourcaud-Trocme N, Ermentrout B, Urban NN. Correlationinduced synchronization of oscillations in olfactory bulb neurons. J Neurosci 26: 3646-3655, 2006.
29. Ginzburg I, Sompolinsky H. Theory of correlations in stochastic neural networks. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 50: 3171-3191, 1994.
30. Gu N, Vervaeke K, Hu H, Storm JF. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715, 2005.
31. Guan D, Higgs M, Horton L, Spain W, Foehring R. Contributions of kv7-mediated potassium current to sub-and suprathreshold responses of rat layer II/III neocortical pyramidal neurons. J Neurophysiol 106: 1722-1733, 2011.
32. Gutnisky DA, Dragoi V. Adaptive coding of visual information in neural populations. Nature 452: 220-224, 2008.
33. Higgs M, Foehring R, Spain W. Conditional burst firing controlled by Kv7 and SK channels in neocortical layer 2/3 pyramidal neurons (Abstract). Soc Neurosci Abstr 33, 2007.
34. Hong S, Lnenicka G. Activity-dependent reduction in voltage-dependent calcium current in a crayfish motoneuron. J Neurosci 15: 3539-3547, 1995.
35. Hong S, Ratte S, Prescott SA, De Schutter E. Single neuron firing properties impact correlation-based population coding. J Neurosci 32: 1413-1428, 2012.
36. Hromadka T, DeWeese MR, Zador AM. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6: e16, 2008.
37. Ibata K, Sun Q, Turrigiano GG. Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57: 819-826, 2008.
38. Jentsch TJ. Neuronal KCNQ potassium channels: physiology and role in disease. Nat Rev Neurosci 1: 21-30, 2000.
39. Josic K, Shea-Brown E, Doiron B, de la Rocha J. Stimulus-dependent correlations and population codes. Neural Comput 21: 2774-2804, 2009.
40. Kohn A. Visual adaptation: physiology, mechanisms, and functional benefits. J Neurophysiol 97: 3155-3164, 2007.
41. Kongden H, Geisler C, Fusi S, Wang XJ, Lscher HR, Giugliano M. The dynamical response properties of neocortical neurons to temporally modulated noisy inputs in vitro. Cereb Cortex 18: 2086-2097, 2008.
42. Lawrence JJ, Saraga F, Churchill JF, Statland JM, Travis KE, Skinner FK, McBain CJ. Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J Neurosci 26: 12325-12338, 2006.
43. Li S, Choi V, Tzounopoulos T. Pathogenic plasticity of kv7.2/3 channel activity is essential for the induction of tinnitus. Proc Natl Acad Sci USA 110: 9980-9985, 2013.
44. Litwin-Kumar A, Oswald AM, Urban NN, Doiron B. Balanced synaptic input shapes the correlation between neural spike trains. PLoS Comput Biol 7: e1002305, 2011.
45. MacLean J, Zhang Y, Johnson BR. Harris-Warrick RM. Activityindependent homeostasis in rhythmically active neurons. Neuron 37: 109-120, 2003.
46. Main M, Cryan J, Dupere J, Cox B, Clare J, Burbudge SA. Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol Pharmacol 58: 253-262, 2000.
47. McCormick DA, Contreras D. On the cellular and network bases of epilepsy. Annu Rev Physiol 63: 815-846, 2001.
48. Muller E, Buesing L, Schemmel J, Meier K. Spike-frequency adapting neural ensembles: beyond mean adaptation and renewal theories. Neural Comput 19: 2950-3010, 2007.
49. Naud R, Gerstner W. Coding and decoding with adapting neurons: a population approach to the peri-stimulus time histogram. PLoS Comput Biol 8: e1002711, 2012.
50. Neubauer BA, Waldegger S, Heinzinger J, Hahn A, Kurlemann G, Fiedler B, Eberhard F, Muhle H, Stephani U, Garkisch S, Eeg-Olofsson O, Müller U, Sander T. KCNQ2 and KCNQ3 mutations contribute to different idiopathic epilepsy syndromes. Neurology 71: 177-183, 2008.
51. Norea AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 183: 137-153, 2003.
52. Passmore GM, Selyanko AA, Mistry M, Al-Qatari M, Marsh SJ, Matthews EA, Dickenson AH, Brown TA, Burbudge SA, Main M, Brown DA. KCNQ/M currents in sensory neurons: significance for pain therapy. J Neurosci 23: 7227-7236, 2003.
53. Peters H, Hu H, Pongs O, Storm J, Isbrandt D. Conditional transgenic suppression of m channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 8: 51-60, 2005.
54. Ping Y, Tsunoda S. Inactivity-induced increase in nAChRs upregulates shal K(+) channels to stabilize synaptic potentials. Nat Neurosci 15: 90-97, 2012.
55. Ransdell JL, Nair SS, Schulz DJ. Rapid homeostatic plasticity of intrinsic excitability in a central pattern generator network stabilizes functional neural network output. J Neurosci 32: 9649-9658, 2012.
56. Ratte S, Hong S, De Schutter E, Prescott SA. Impact of neuronal properties on network coding: roles of spike initiation dynamics and robust synchrony transfer. Neuron 78: 758-772, 2013.
57. Richardson M. Firing-rate response of linear and nonlinear integrate-and-fire neurons to modulated current-based and conductance-based synaptic drive. Phys Rev E Stat Nonlin Soft Matter Phys 76: 021919, 2007.
58. Richardson M. Dynamics of neurons and networks of neurons with voltageactivated and calcium-activated current. Phys Rev E Stat Nonlin Soft Matter Phys 80: 021928, 2009.
59. Risken H. The Fokker-Planck Equation: Methods of Solution and Applications (3rd ed). New York: Springer-Verlag, 1996.
60. Rosenbaum R, Josic K. Membrane potential and spike train statistics depend distinctly on input statistics. Phys Rev E Stat Nonlin Soft Matter Phys 84: 051902, 2011.
61. Rosenbaum R, Rubin JE, Doiron B. Short-term synaptic depression and stochastic vesicle dynamics reduce and shape neuronal correlations. J Neurophysiol 109: 475-484, 2013.
62. Schwalger T, Fisch K, Benda J, Lindner B. How noisy adaptation of neurons shapes interspike interval histograms and correlations. PLoS Comput Biol 6: e1001026, 2010.
63. Selyanko AA, Hadley J, Brown DA. Properties of single M-type KNCQ2/ KCNQ3 potassium chanels expressed in mammalian cells. J Physiol 534: 15-24, 2001.
64. Shah NH, Aizenman E. Voltage-gated potassium channels at the crossroads of neuronal function, ischemic tolerance, and neurodegeneration. Transl Stroke Res 5: 38-58, 2014.
65. Shea-Brown E, Josic K, de la Rocha J, Doiron B. Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. Phys Rev Lett 100: 108102, 2008.
66. Soldovieri MV, Castaldo P, Iodice L, Miceli F, Barrese V, Bellini G, Miraglia del Giudice E, Pascotto A, Bonatti S, Annunziato L, Taglialatela M. Decreased subunit stability as a novel mechanism for potassium current impairment by a KCNQ2 c terminus mutation causing benign familial neonatal convulsions. J Biol Chem 281: 418-428, 2006.
67. Sompolinsky H, Yoon H, Kang K, Shamir M. Population coding in neuronal systems with correlated noise. Phys Rev E Stat Nonlin Soft Matter Phys 64: 051904, 2001.
68. Stafstrom CE. Persistent sodium current and its role in epilepsy. Epilepsy Curr 7: 15-22, 2007.
69. Tatulian L, Delmas P, Abogadie F, Brown D. Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the novel anti-convulsant drug retigabine. J Neurosci 21: 5535-5545, 2001.
70. Tchumatchenko T, Malyshev A, Geisel T, Volgushev M, Wolf F. Correlations and synchrony in threshold neuron models. Phys Rev Lett 104: 058102, 2010.
71. Toyoizumi T, Rad KR, Paninski L. Mean-field approximations for coupled populations of generalized linear model spiking neurons with Markov refractoriness. Neural Comput 21: 1203-1243, 2008.
72. Trousdale J, Hu Y, Shea-Brown E, Josic K. Impact of network structure and cellular response on spike time correlations. PLoS Comput Biol 8: e1002408, 2012.
73. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. Activitydependent scaling of quantal amplitude in neocortical neurons. Nature 361: 892-896, 1998.
74. van Welie I, van Hooft J, Wadman W. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated IH channels. Proc Natl Acad Sci USA 101: 5123-5128, 2004.
75. Vilela RD, Lindner B. Comparative study of different integrate-and-fire neurons: spontaneous activity, dynamical response, and stimulus-induced correlation. Phys Rev E Stat Nonlin Soft Matter Phys 80: 031909, 2009.
76. Wang H, Pan A, Shi W, Brown B, Wymore R, Cohen I, Dixon J, McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the m-channel. Science 282: 1890-1893, 1998.
77. Wang Y, Iliescu BF, Ma J, Josic K, Dragoi V. Adaptive changes in neuronal synchronization in macaque v4. J Neurosci 31: 13204-13213, 2011.
78. Wuttke TV, Jurkat-Rott K, Paulus W, Garncarek M, Lehmann-Horn F, Lerche H. Peripheral nerve hyperexcitability due to dominant-negative KCNQ2 mutations. Neurology 69: 2045-2053, 2007.
79. Zheng Q, Fang D, Liu M, Cai J, Wan Y, Han JS, Xing GG. Suppression of KCNQ/M (kv7) potassium channels in dorsal root ganglion neurons contributes to the development of bone cancer pain in a rat model. Pain 154: 434-448, 2012.